Advancement in the relationship between gut microbiota and coronary artery disease_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

LIU Kaiwen ¹ , ZHANG Kui ² , ZHOU Ning ² ,  DONG Ran ²

1. Capital Medical University, Beijing, 100069, P. R. China;
2. Department of Cardiac Surgery, Beijing Anzhen Hospital Affiliated to Capital Medical University, Beijing, 100029, P. R. China;

Corresponding author：

DONG Ran, Email: dongran6618@hotmail.com

Keywords：

Coronary artery disease; gut microbiota; atherosclerosis; trimethylamine N-oxide; review

DOI：

10.7507/1007-4848.202212032

Video：

Export PDF Favorites Scan Get Citation

Abstract Full text Figures/Tables Video References Cited by

Including gut microbiota and oral microbiota, various microorganisms in different human ecosystem constitute the human microbiota, which play an important role in human metabolism, immunity and maintaining microecological homeostasis. Abnormal changes in gut microbiota known as dysbiosis may lead to metabolic abnormalities and inflammatory changes, which are closely related to disease states including hypertension, diabetes, inflammatory bowel disease, and autoimmune diseases. The main cause of coronary artery disease is coronary atherosclerosis, a chronic and progressive inflammatory disease. Many evidences have shown that there is a correlation between gut microbiota and coronary artery disease. Therefore, we aim to review the relationship between gut microbiota and coronary artery disease, and discuss the possible research directions and application prospects.

Citation： LIU Kaiwen, ZHANG Kui, ZHOU Ning, DONG Ran. Advancement in the relationship between gut microbiota and coronary artery disease. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2023, 30(5): 746-752. doi: 10.7507/1007-4848.202212032 Copy

1.	Sigvant B, Hasvold P, Thuresson M, et al. Myocardial infarction and peripheral arterial disease: Treatment patterns and long-term outcome in men and women results from a Swedish nationwide study. Eur J Prev Cardiol, 2021, 28(13): 1426-1434.
2.	Roberts AB, Gu X, Buffa JA, et al. Development of a gut microbe-targeted nonlethal therapeutic to inhibit thrombosis potential. Nat Med, 2018, 24(9): 1407-1417.
3.	Marques FZ, Mackay CR, Kaye DM. Beyond gut feelings: How the gut microbiota regulates blood pressure. Nat Rev Cardiol, 2018, 15(1): 20-32.
4.	Kim J, Lee H, An J, et al. Alterations in gut microbiota by statin therapy and possible intermediate effects on hyperglycemia and hyperlipidemia. Front Microbiol, 2019, 10: 1947.
5.	Ni J, Wu GD, Albenberg L, et al. Gut microbiota and IBD: Causation or correlation? Nat Rev Gastroenterol Hepatol, 2017, 14(10): 573-584.
6.	Barko PC, McMichael MA, Swanson KS, et al. The gastrointestinal microbiome: A review. J Vet Intern Med, 2018, 32(1): 9-25.
7.	Sender R, Fuchs S, Milo R. Revised estimates for the number of human and bacteria cells in the body. PLoS Biol, 2016, 14(8): e1002533.
8.	Ramírez-Macías I, Orenes-Piñero E, Camelo-Castillo A, et al. Novel insights in the relationship of gut microbiota and coronary artery diseases. Crit Rev Food Sci Nutr, 2022, 62(14): 3738-3750.
9.	Arumugam M, Raes J, Pelletier E, et al. Enterotypes of the human gut microbiome. Nature, 2011, 473(7346): 174-180.
10.	Emoto T, Yamashita T, Sasaki N, et al. Analysis of gut microbiota in coronary artery disease patients: A possible link between gut microbiota and coronary artery disease. J Atheroscler Thromb, 2016, 23(8): 908-921.
11.	Cui L, Zhao T, Hu H, et al. Association study of gut flora in coronary heart disease through high-throughput sequencing. Biomed Res Int, 2017, 2017: 3796359.
12.	Yoshida N, Emoto T, Yamashita T, et al. Bacteroides vulgatus and bacteroides dorei reduce gut microbial lipopolysaccharide production and inhibit atherosclerosis. Circulation, 2018, 138(22): 2486-2498.
13.	Zhu Q, Gao R, Zhang Y, et al. Dysbiosis signatures of gut microbiota in coronary artery disease. Physiol Genomics, 2018, 50(10): 893-903.
14.	Toya T, Corban MT, Marrietta E, et al. Coronary artery disease is associated with an altered gut microbiome composition. PLoS One, 2020, 15(1): e0227147.
15.	Yoshida N, Sasaki K, Sasaki D, et al. Effect of resistant starch on the gut microbiota and its metabolites in patients with coronary artery disease. J Atheroscler Thromb, 2019, 26(8): 705-719.
16.	Tuomisto S, Huhtala H, Martiskainen M, et al. Age-dependent association of gut bacteria with coronary atherosclerosis: Tampere Sudden Death Study. PLoS One, 2019, 14(8): e0221345.
17.	Nakajima A, Mitomo S, Yuki H, et al. Gut microbiota and coronary plaque characteristics. J Am Heart Assoc, 2022, 11(17): e026036.
18.	Janssens Y, Nielandt J, Bronselaer A, et al. Disbiome database: Linking the microbiome to disease. BMC Microbiol, 2018, 18(1): 50.
19.	Liu H, Chen X, Hu X, et al. Alterations in the gut microbiome and metabolism with coronary artery disease severity. Microbiome, 2019, 7(1): 68.
20.	Chittim CL, Martínez Del Campo A, et al. Gut bacterial phospholipase Ds support disease-associated metabolism by generating choline. Nat Microbiol, 2019, 4(1): 155-163.
21.	Falony G, Vieira-Silva S, Raes J. Microbiology meets big data: The case of gut microbiota-derived trimethylamine. Annu Rev Microbiol, 2015, 69: 305-321.
22.	Zeisel SH, Warrier M. Trimethylamine N-Oxide, the microbiome, and heart and kidney disease. Annu Rev Nutr, 2017, 37: 157-181.
23.	Bogiatzi C, Gloor G, Allen-Vercoe E, et al. Metabolic products of the intestinal microbiome and extremes of atherosclerosis. Atherosclerosis, 2018, 273: 91-97.
24.	Amrein M, Li XS, Walter J, et al. Gut microbiota-dependent metabolite trimethylamine N-oxide (TMAO) and cardiovascular risk in patients with suspected functionally relevant coronary artery disease (fCAD). Clin Res Cardiol, 2022, 111(6): 692-704.
25.	Senthong V, Wang Z, Li XS, et al. Intestinal microbiota-generated metabolite trimethylamine-N-oxide and 5-year mortality risk in stable coronary artery disease: The contributory role of intestinal microbiota in a COURAGE-like patient cohort. J Am Heart Assoc, 2016, 5(6): e002816.
26.	Tang WHW, Li XS, Wu Y, et al. Plasma trimethylamine N-oxide (TMAO) levels predict future risk of coronary artery disease in apparently healthy individuals in the EPIC-Norfolk prospective population study. Am Heart J, 2021, 236: 80-86.
27.	Meyer KA, Benton TZ, Bennett BJ, et al. Microbiota-dependent metabolite trimethylamine N-oxide and coronary artery calcium in the Coronary Artery Risk Development in Young Adults Study (CARDIA). J Am Heart Assoc, 2016, 5(10): e003970.
28.	Koay YC, Chen YC, Wali JA, et al. Plasma levels of trimethylamine-N-oxide can be increased with 'healthy' and 'unhealthy' diets and do not correlate with the extent of atherosclerosis but with plaque instability. Cardiovasc Res, 2021, 117(2): 435-449.
29.	Al-Obaide MAI, Singh R, Datta P, et al. Gut microbiota-dependent trimethylamine-N-oxide and serum biomarkers in patients with T2DM and advanced CKD. J Clin Med, 2017, 6(9): 86.
30.	Zhu W, Gregory JC, Org E, et al. Gut microbial metabolite TMAO enhances platelet hyperreactivity and thrombosis risk. Cell, 2016, 165(1): 111-124.
31.	Wu P, Chen J, Chen J, et al. Trimethylamine N-oxide promotes apoE-/- mice atherosclerosis by inducing vascular endothelial cell pyroptosis via the SDHB/ROS pathway. J Cell Physiol, 2020, 235(10): 6582-6591.
32.	Chong Nguyen C, Duboc D, Rainteau D, et al. Circulating bile acids concentration is predictive of coronary artery disease in human. Sci Rep, 2021, 11(1): 22661.
33.	Mayerhofer CCK, Ueland T, Broch K, et al. Increased secondary/primary bile acid ratio in chronic heart failure. J Card Fail, 2017, 23(9): 666-671.
34.	Liu H, Tian R, Wang H, et al. Gut microbiota from coronary artery disease patients contributes to vascular dysfunction in mice by regulating bile acid metabolism and immune activation. J Transl Med, 2020, 18(1): 382.
35.	Jadoon A, Mathew AV, Byun J, et al. Gut microbial product predicts cardiovascular risk in chronic kidney disease patients. Am J Nephrol, 2018, 48(4): 269-277.
36.	Jie Z, Xia H, Zhong SL, et al. The gut microbiome in atherosclerotic cardiovascular disease. Nat Commun, 2017, 8(1): 845.
37.	Krishnan S, Alden N, Lee K. Pathways and functions of gut microbiota metabolism impacting host physiology. Curr Opin Biotechnol, 2015, 36: 137-145.
38.	Ivashkin VT, Kashukh YA. Impact of L-carnitine and phosphatidylcholine containing products on the proatherogenic metabolite TMAO production and gut microbiome changes in patients with coronary artery disease. Vopr Pitan, 2019, 88(4): 25-33.
39.	Ma Y, Zhu L, Ma Z, et al. Distinguishing feature of gut microbiota in Tibetan highland coronary artery disease patients and its link with diet. Sci Rep, 2021, 11(1): 18486.
40.	Stewart RAH. Primary prevention of cardiovascular disease with a mediterranean diet supplemented with extra-virgin olive oil or nuts. N Engl J Med, 2018, 379(14): 1388.
41.	Garcia-Mantrana I, Selma-Royo M, Alcantara C, et al. Shifts on gut microbiota associated to mediterranean diet adherence and specific dietary intakes on general adult population. Front Microbiol, 2018, 9: 890.
42.	Khan TJ, Ahmed YM, Zamzami MA, et al. Effect of atorvastatin on the gut microbiota of high fat diet-induced hypercholesterolemic rats. Sci Rep, 2018, 8(1): 662.
43.	Vieira-Silva S, Falony G, Belda E, et al. Statin therapy is associated with lower prevalence of gut microbiota dysbiosis. Nature, 2020, 581(7808): 310-315.
44.	Wang L, Zhou W, Guo M, et al. The gut microbiota is associated with clinical response to statin treatment in patients with coronary artery disease. Atherosclerosis, 2021, 325: 16-23.
45.	Yang Q, Xu Y, Shen L, et al. Guanxinning tablet attenuates coronary atherosclerosis via regulating the gut microbiota and their metabolites in tibetan minipigs induced by a high-fat diet. J Immunol Res, 2022, 2022: 7128230.
46.	Suez J, Zmora N, Segal E, et al. The pros, cons, and many unknowns of probiotics. Nat Med, 2019, 25(5): 716-729.
47.	Sun B, Ma T, Li Y, et al. Bifidobacterium lactis probio-M8 adjuvant treatment confers added benefits to patients with coronary artery disease via target modulation of the gut-heart/-brain axes. mSystems, 2022, 7(2): e0010022.
48.	Malik M, Suboc TM, Tyagi S, et al. Lactobacillus plantarum 299v supplementation improves vascular endothelial function and reduces inflammatory biomarkers in men with stable coronary artery disease. Circ Res, 2018, 123(9): 1091-1102.
49.	Cosola C, De Angelis M, Rocchetti MT, et al. Beta-glucans supplementation associates with reduction in P-Cresyl sulfate levels and improved endothelial vascular reactivity in healthy individuals. PLoS One, 2017, 12(1): e0169635.
50.	Chen PB, Black AS, Sobel AL, et al. Directed remodeling of the mouse gut microbiome inhibits the development of atherosclerosis. Nat Biotechnol, 2020, 38(11): 1288-1297.
51.	Gregory JC, Buffa JA, Org E, et al. Transmission of atherosclerosis susceptibility with gut microbial transplantation. J Biol Chem, 2015, 290(9): 5647-5660.
52.	Khoruts A, Sadowsky MJ. Understanding the mechanisms of faecal microbiota transplantation. Nat Rev Gastroenterol Hepatol, 2016, 13(9): 508-516.
53.	Emoto T, Yamashita T, Kobayashi T, et al. Characterization of gut microbiota profiles in coronary artery disease patients using data mining analysis of terminal restriction fragment length polymorphism: Gut microbiota could be a diagnostic marker of coronary artery disease. Heart Vessels, 2017, 32(1): 39-46.
54.	Zheng YY, Wu TT, Liu ZQ, et al. Gut microbiome-based diagnostic model to predict coronary artery disease. J Agric Food Chem, 2020, 68(11): 3548-3557.

1. Sigvant B, Hasvold P, Thuresson M, et al. Myocardial infarction and peripheral arterial disease: Treatment patterns and long-term outcome in men and women results from a Swedish nationwide study. Eur J Prev Cardiol, 2021, 28(13): 1426-1434.
2. Roberts AB, Gu X, Buffa JA, et al. Development of a gut microbe-targeted nonlethal therapeutic to inhibit thrombosis potential. Nat Med, 2018, 24(9): 1407-1417.
3. Marques FZ, Mackay CR, Kaye DM. Beyond gut feelings: How the gut microbiota regulates blood pressure. Nat Rev Cardiol, 2018, 15(1): 20-32.
4. Kim J, Lee H, An J, et al. Alterations in gut microbiota by statin therapy and possible intermediate effects on hyperglycemia and hyperlipidemia. Front Microbiol, 2019, 10: 1947.
5. Ni J, Wu GD, Albenberg L, et al. Gut microbiota and IBD: Causation or correlation? Nat Rev Gastroenterol Hepatol, 2017, 14(10): 573-584.
6. Barko PC, McMichael MA, Swanson KS, et al. The gastrointestinal microbiome: A review. J Vet Intern Med, 2018, 32(1): 9-25.
7. Sender R, Fuchs S, Milo R. Revised estimates for the number of human and bacteria cells in the body. PLoS Biol, 2016, 14(8): e1002533.
8. Ramírez-Macías I, Orenes-Piñero E, Camelo-Castillo A, et al. Novel insights in the relationship of gut microbiota and coronary artery diseases. Crit Rev Food Sci Nutr, 2022, 62(14): 3738-3750.
9. Arumugam M, Raes J, Pelletier E, et al. Enterotypes of the human gut microbiome. Nature, 2011, 473(7346): 174-180.
10. Emoto T, Yamashita T, Sasaki N, et al. Analysis of gut microbiota in coronary artery disease patients: A possible link between gut microbiota and coronary artery disease. J Atheroscler Thromb, 2016, 23(8): 908-921.
11. Cui L, Zhao T, Hu H, et al. Association study of gut flora in coronary heart disease through high-throughput sequencing. Biomed Res Int, 2017, 2017: 3796359.
12. Yoshida N, Emoto T, Yamashita T, et al. Bacteroides vulgatus and bacteroides dorei reduce gut microbial lipopolysaccharide production and inhibit atherosclerosis. Circulation, 2018, 138(22): 2486-2498.
13. Zhu Q, Gao R, Zhang Y, et al. Dysbiosis signatures of gut microbiota in coronary artery disease. Physiol Genomics, 2018, 50(10): 893-903.
14. Toya T, Corban MT, Marrietta E, et al. Coronary artery disease is associated with an altered gut microbiome composition. PLoS One, 2020, 15(1): e0227147.
15. Yoshida N, Sasaki K, Sasaki D, et al. Effect of resistant starch on the gut microbiota and its metabolites in patients with coronary artery disease. J Atheroscler Thromb, 2019, 26(8): 705-719.
16. Tuomisto S, Huhtala H, Martiskainen M, et al. Age-dependent association of gut bacteria with coronary atherosclerosis: Tampere Sudden Death Study. PLoS One, 2019, 14(8): e0221345.
17. Nakajima A, Mitomo S, Yuki H, et al. Gut microbiota and coronary plaque characteristics. J Am Heart Assoc, 2022, 11(17): e026036.
18. Janssens Y, Nielandt J, Bronselaer A, et al. Disbiome database: Linking the microbiome to disease. BMC Microbiol, 2018, 18(1): 50.
19. Liu H, Chen X, Hu X, et al. Alterations in the gut microbiome and metabolism with coronary artery disease severity. Microbiome, 2019, 7(1): 68.
20. Chittim CL, Martínez Del Campo A, et al. Gut bacterial phospholipase Ds support disease-associated metabolism by generating choline. Nat Microbiol, 2019, 4(1): 155-163.
21. Falony G, Vieira-Silva S, Raes J. Microbiology meets big data: The case of gut microbiota-derived trimethylamine. Annu Rev Microbiol, 2015, 69: 305-321.
22. Zeisel SH, Warrier M. Trimethylamine N-Oxide, the microbiome, and heart and kidney disease. Annu Rev Nutr, 2017, 37: 157-181.
23. Bogiatzi C, Gloor G, Allen-Vercoe E, et al. Metabolic products of the intestinal microbiome and extremes of atherosclerosis. Atherosclerosis, 2018, 273: 91-97.
24. Amrein M, Li XS, Walter J, et al. Gut microbiota-dependent metabolite trimethylamine N-oxide (TMAO) and cardiovascular risk in patients with suspected functionally relevant coronary artery disease (fCAD). Clin Res Cardiol, 2022, 111(6): 692-704.
25. Senthong V, Wang Z, Li XS, et al. Intestinal microbiota-generated metabolite trimethylamine-N-oxide and 5-year mortality risk in stable coronary artery disease: The contributory role of intestinal microbiota in a COURAGE-like patient cohort. J Am Heart Assoc, 2016, 5(6): e002816.
26. Tang WHW, Li XS, Wu Y, et al. Plasma trimethylamine N-oxide (TMAO) levels predict future risk of coronary artery disease in apparently healthy individuals in the EPIC-Norfolk prospective population study. Am Heart J, 2021, 236: 80-86.
27. Meyer KA, Benton TZ, Bennett BJ, et al. Microbiota-dependent metabolite trimethylamine N-oxide and coronary artery calcium in the Coronary Artery Risk Development in Young Adults Study (CARDIA). J Am Heart Assoc, 2016, 5(10): e003970.
28. Koay YC, Chen YC, Wali JA, et al. Plasma levels of trimethylamine-N-oxide can be increased with 'healthy' and 'unhealthy' diets and do not correlate with the extent of atherosclerosis but with plaque instability. Cardiovasc Res, 2021, 117(2): 435-449.
29. Al-Obaide MAI, Singh R, Datta P, et al. Gut microbiota-dependent trimethylamine-N-oxide and serum biomarkers in patients with T2DM and advanced CKD. J Clin Med, 2017, 6(9): 86.
30. Zhu W, Gregory JC, Org E, et al. Gut microbial metabolite TMAO enhances platelet hyperreactivity and thrombosis risk. Cell, 2016, 165(1): 111-124.
31. Wu P, Chen J, Chen J, et al. Trimethylamine N-oxide promotes apoE-/- mice atherosclerosis by inducing vascular endothelial cell pyroptosis via the SDHB/ROS pathway. J Cell Physiol, 2020, 235(10): 6582-6591.
32. Chong Nguyen C, Duboc D, Rainteau D, et al. Circulating bile acids concentration is predictive of coronary artery disease in human. Sci Rep, 2021, 11(1): 22661.
33. Mayerhofer CCK, Ueland T, Broch K, et al. Increased secondary/primary bile acid ratio in chronic heart failure. J Card Fail, 2017, 23(9): 666-671.
34. Liu H, Tian R, Wang H, et al. Gut microbiota from coronary artery disease patients contributes to vascular dysfunction in mice by regulating bile acid metabolism and immune activation. J Transl Med, 2020, 18(1): 382.
35. Jadoon A, Mathew AV, Byun J, et al. Gut microbial product predicts cardiovascular risk in chronic kidney disease patients. Am J Nephrol, 2018, 48(4): 269-277.
36. Jie Z, Xia H, Zhong SL, et al. The gut microbiome in atherosclerotic cardiovascular disease. Nat Commun, 2017, 8(1): 845.
37. Krishnan S, Alden N, Lee K. Pathways and functions of gut microbiota metabolism impacting host physiology. Curr Opin Biotechnol, 2015, 36: 137-145.
38. Ivashkin VT, Kashukh YA. Impact of L-carnitine and phosphatidylcholine containing products on the proatherogenic metabolite TMAO production and gut microbiome changes in patients with coronary artery disease. Vopr Pitan, 2019, 88(4): 25-33.
39. Ma Y, Zhu L, Ma Z, et al. Distinguishing feature of gut microbiota in Tibetan highland coronary artery disease patients and its link with diet. Sci Rep, 2021, 11(1): 18486.
40. Stewart RAH. Primary prevention of cardiovascular disease with a mediterranean diet supplemented with extra-virgin olive oil or nuts. N Engl J Med, 2018, 379(14): 1388.
41. Garcia-Mantrana I, Selma-Royo M, Alcantara C, et al. Shifts on gut microbiota associated to mediterranean diet adherence and specific dietary intakes on general adult population. Front Microbiol, 2018, 9: 890.
42. Khan TJ, Ahmed YM, Zamzami MA, et al. Effect of atorvastatin on the gut microbiota of high fat diet-induced hypercholesterolemic rats. Sci Rep, 2018, 8(1): 662.
43. Vieira-Silva S, Falony G, Belda E, et al. Statin therapy is associated with lower prevalence of gut microbiota dysbiosis. Nature, 2020, 581(7808): 310-315.
44. Wang L, Zhou W, Guo M, et al. The gut microbiota is associated with clinical response to statin treatment in patients with coronary artery disease. Atherosclerosis, 2021, 325: 16-23.
45. Yang Q, Xu Y, Shen L, et al. Guanxinning tablet attenuates coronary atherosclerosis via regulating the gut microbiota and their metabolites in tibetan minipigs induced by a high-fat diet. J Immunol Res, 2022, 2022: 7128230.
46. Suez J, Zmora N, Segal E, et al. The pros, cons, and many unknowns of probiotics. Nat Med, 2019, 25(5): 716-729.
47. Sun B, Ma T, Li Y, et al. Bifidobacterium lactis probio-M8 adjuvant treatment confers added benefits to patients with coronary artery disease via target modulation of the gut-heart/-brain axes. mSystems, 2022, 7(2): e0010022.
48. Malik M, Suboc TM, Tyagi S, et al. Lactobacillus plantarum 299v supplementation improves vascular endothelial function and reduces inflammatory biomarkers in men with stable coronary artery disease. Circ Res, 2018, 123(9): 1091-1102.
49. Cosola C, De Angelis M, Rocchetti MT, et al. Beta-glucans supplementation associates with reduction in P-Cresyl sulfate levels and improved endothelial vascular reactivity in healthy individuals. PLoS One, 2017, 12(1): e0169635.
50. Chen PB, Black AS, Sobel AL, et al. Directed remodeling of the mouse gut microbiome inhibits the development of atherosclerosis. Nat Biotechnol, 2020, 38(11): 1288-1297.
51. Gregory JC, Buffa JA, Org E, et al. Transmission of atherosclerosis susceptibility with gut microbial transplantation. J Biol Chem, 2015, 290(9): 5647-5660.
52. Khoruts A, Sadowsky MJ. Understanding the mechanisms of faecal microbiota transplantation. Nat Rev Gastroenterol Hepatol, 2016, 13(9): 508-516.
53. Emoto T, Yamashita T, Kobayashi T, et al. Characterization of gut microbiota profiles in coronary artery disease patients using data mining analysis of terminal restriction fragment length polymorphism: Gut microbiota could be a diagnostic marker of coronary artery disease. Heart Vessels, 2017, 32(1): 39-46.
54. Zheng YY, Wu TT, Liu ZQ, et al. Gut microbiome-based diagnostic model to predict coronary artery disease. J Agric Food Chem, 2020, 68(11): 3548-3557.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Advancement in the relationship between gut microbiota and coronary artery disease

Abstract Full text Figures/Tables Video References Cited by

Previous Article

Next Article

Format

Content